Beyond fruit flies: the diversity of small RNAs across arthropods

Small RNA molecules called piRNAs are vital in regulating the activity of the genome, but most piRNA studies have focused on model organisms. By sequencing small RNAs from 20 arthropods, we discovered that piRNAs have a surprisingly dynamic evolutionary history.

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Horseshoe crabs are undeniably strange animals. They have ten eyes, blue blood, and five pairs of legs underneath a hard domed shell (Figure 1). But this bizarre anatomy is just one example of the diversity found in the arthropods, a group of animals that includes arachnids, centipedes, crustaceans and insects. It is thought that there are over 5 million arthropod species, and they show an astonishing array of physiology, behaviour and life cycles. However, our knowledge of the genetics of arthropods is mainly based on one species: the fruit fly Drosophila melanogaster.

Figure 1: Atlantic horseshoe crabs are just one example of the diversity found across arthropods

Fruit flies are a favourite for genetic studies because they are easy to manipulate genetically, allowing tightly-controlled experiments that reveal the details of genetic pathways. One such pathway is the small RNA mechanism, where small strands of RNA regulate the activity of other DNA or RNA molecules. A major target of small RNAs are transposons (also known as “jumping genes”), which copy themselves into other parts of the genome and alter the sequence of genes. In fruit flies, a particular type of small RNA called piRNAs are found in the reproductive tissues, and primarily protect the flies against transposons that can disrupt their genes and cause sterility. Based on these fruit fly studies, and similar results in nematodes and mice, piRNAs have been assumed to be restricted to reproductive tissues in all animals. Recently, however, they have been found throughout the whole body of mosquitoes, targeting transposons and viruses.

These findings raised an important question for us - if piRNAs are found throughout the body in mosquitoes, why not other arthropods? To approach this question systematically, we chose 20 species from across the arthropod tree of life: three chelicerates (horseshoe crab, house spider and bark scorpion), a centipede, a crustacean (woodlouse), and 15 insects. To catch each species, we relied on a network of collaborators working across three continents, ranging from cold Scottish beaches to the Arizona desert (Figure 2). For each species we took samples from reproductive and non-reproductive tissues, and sequenced the small RNAs from each sample. By mapping these small RNAs to the genome and analysing their length and sequence, we could test whether piRNAs were found outside the reproductive tissues, and if so what they were targeting.

Figure 3: piRNAs are found throughout the body of most arthropods (top 3 rows), but restricted to reproductive tissue in some species (bottom row)

Our results revealed that piRNAs are present throughout the body in the vast majority of arthropods - in fact, the only species where they are restricted to reproductive tissues are woodlice, bumblebees, burying beetles and fruit flies (Figure 3). In the other species, piRNAs target transposons throughout the body, as well as genes and viruses in some species. Matching these patterns to the arthropod tree of life revealed that piRNAs were likely present throughout the body in the common ancestor of all arthropods more than 500 million years ago, and have specialized to reproductive tissues independently in particular lineages. These results hint that the molecular biology of arthropods may be every bit as diverse as their morphology and ecology.

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Limulus polyphemus by U.S. Fish and Wildlife Service Northeast Region (Horseshoe Crab) [CC BY 2.0 (http://creativecommons.org/licenses/by/2.0) or Public domain], via Wikimedia Commons

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